Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)

Common buckwheat (Fagopyrum esculentum) is a heteromorphic self-incompatible (SI) species with two types of floral architecture: thrum (short style) and pin (long style). The floral morphology and intra-morph incompatibility are controlled by a single genetic locus, S. However, the molecular mechani...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Heredity 2019-10, Vol.123 (4), p.492-502
Hauptverfasser: Takeshima, Ryoma, Nishio, Takeshi, Komatsu, Setsuko, Kurauchi, Nobuyuki, Matsui, Katsuhiro
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 502
container_issue 4
container_start_page 492
container_title Heredity
container_volume 123
creator Takeshima, Ryoma
Nishio, Takeshi
Komatsu, Setsuko
Kurauchi, Nobuyuki
Matsui, Katsuhiro
description Common buckwheat (Fagopyrum esculentum) is a heteromorphic self-incompatible (SI) species with two types of floral architecture: thrum (short style) and pin (long style). The floral morphology and intra-morph incompatibility are controlled by a single genetic locus, S. However, the molecular mechanisms underlying the heteromorphic self-incompatibility of common buckwheat remain unclear. To identify these mechanisms, we performed proteomic, quantitative reverse-transcription PCR, and linkage analyses. Comparison of protein profiles between the long and short styles revealed a protein unique to the short style. Amino-acid sequencing revealed that it was a truncated form of polygalacturonase (PG); we designated the gene encoding this protein FePG1. Phylogenetic analysis classified FePG1 into the same clade as PGs that function in pollen development and floral morphology. FePG1 expression was significantly higher in short styles than in long styles. It was expressed in flowers of a short-homostyle line but not in flowers of a long-homostyle line. Linkage analysis indicated that FePG1 was not linked to the S locus; it could be a factor downstream of this locus. Our finding of a gene putatively working under the regulation of the S locus provides useful information for elucidation of the mechanism of heteromorphic self-incompatibility.
doi_str_mv 10.1038/s41437-019-0227-x
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6781162</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2288675008</sourcerecordid><originalsourceid>FETCH-LOGICAL-c537t-3c075d454a99cbc5420e6976c0f2f24d88a33a1541f03e94985e0eb29b9dbf893</originalsourceid><addsrcrecordid>eNpdkc1u1DAUhSMEotPCA7BBlti0i8D1T2J7g1RVFCpVYgMSO8txnBkXxw52ApOn4JXxMKUCVrZ1zzm-R19VvcDwGgMVbzLDjPIasKyBEF7vH1UbTNumJg2Dx9UGAIsaWv7lpDrN-Q4AKCfyaXVCMfC2ZXJT_bzpbZjd4IyeXQwoDkijrQ0W2WBi78IWTdGvW-21mZcUg85ltJ-Szdn2KE_W_DZ7vyIXUN7FNKM8r97mw7t3h3tcMjJxHEt-t5ivP3ZWz-j8Wm_jtKZlRDabxZc1lvHiWfVk0D7b5_fnWfX5-t2nqw_17cf3N1eXt7VpKJ9raoA3PWuYltJ0pmEEbCt5a2AgA2G9EJpSjRuGB6BWMikaC7YjspN9NwhJz6q3x9xp6Ubbm_J70l5NyY06rSpqp_6dBLdT2_hdtVxg3JIScH4fkOK3xeZZjS4b670OtvRVhFAsgRc-RfrqP-ldXFIo9YpKiJY3AKKo8FFlUsw52eFhGQzqgFsdcauCWx1wq33xvPy7xYPjD1_6C0pAqqQ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2288675008</pqid></control><display><type>article</type><title>Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)</title><source>MEDLINE</source><source>Nature</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><source>SpringerLink Journals - AutoHoldings</source><creator>Takeshima, Ryoma ; Nishio, Takeshi ; Komatsu, Setsuko ; Kurauchi, Nobuyuki ; Matsui, Katsuhiro</creator><creatorcontrib>Takeshima, Ryoma ; Nishio, Takeshi ; Komatsu, Setsuko ; Kurauchi, Nobuyuki ; Matsui, Katsuhiro</creatorcontrib><description>Common buckwheat (Fagopyrum esculentum) is a heteromorphic self-incompatible (SI) species with two types of floral architecture: thrum (short style) and pin (long style). The floral morphology and intra-morph incompatibility are controlled by a single genetic locus, S. However, the molecular mechanisms underlying the heteromorphic self-incompatibility of common buckwheat remain unclear. To identify these mechanisms, we performed proteomic, quantitative reverse-transcription PCR, and linkage analyses. Comparison of protein profiles between the long and short styles revealed a protein unique to the short style. Amino-acid sequencing revealed that it was a truncated form of polygalacturonase (PG); we designated the gene encoding this protein FePG1. Phylogenetic analysis classified FePG1 into the same clade as PGs that function in pollen development and floral morphology. FePG1 expression was significantly higher in short styles than in long styles. It was expressed in flowers of a short-homostyle line but not in flowers of a long-homostyle line. Linkage analysis indicated that FePG1 was not linked to the S locus; it could be a factor downstream of this locus. Our finding of a gene putatively working under the regulation of the S locus provides useful information for elucidation of the mechanism of heteromorphic self-incompatibility.</description><identifier>ISSN: 0018-067X</identifier><identifier>EISSN: 1365-2540</identifier><identifier>DOI: 10.1038/s41437-019-0227-x</identifier><identifier>PMID: 31076649</identifier><language>eng</language><publisher>England: Springer Nature B.V</publisher><subject>Amino acids ; Buckwheat ; Fagopyrum - genetics ; Fagopyrum - growth &amp; development ; Fagopyrum esculentum ; Flowers ; Flowers - genetics ; Flowers - growth &amp; development ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Plant - genetics ; Genetic Linkage - genetics ; Genetic Loci - genetics ; Incompatibility ; Linkage analysis ; Loci ; Molecular modelling ; Morphology ; Phylogeny ; Plant Proteins - genetics ; Pollen ; Pollen - genetics ; Pollen - growth &amp; development ; Polygalacturonase ; Polygalacturonase - genetics ; Proteins ; Proteomics ; Self-incompatibility ; Styles</subject><ispartof>Heredity, 2019-10, Vol.123 (4), p.492-502</ispartof><rights>The Author(s) 2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c537t-3c075d454a99cbc5420e6976c0f2f24d88a33a1541f03e94985e0eb29b9dbf893</citedby><cites>FETCH-LOGICAL-c537t-3c075d454a99cbc5420e6976c0f2f24d88a33a1541f03e94985e0eb29b9dbf893</cites><orcidid>0000-0002-2525-7334 ; 0000-0003-0965-2892</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781162/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781162/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31076649$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Takeshima, Ryoma</creatorcontrib><creatorcontrib>Nishio, Takeshi</creatorcontrib><creatorcontrib>Komatsu, Setsuko</creatorcontrib><creatorcontrib>Kurauchi, Nobuyuki</creatorcontrib><creatorcontrib>Matsui, Katsuhiro</creatorcontrib><title>Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)</title><title>Heredity</title><addtitle>Heredity (Edinb)</addtitle><description>Common buckwheat (Fagopyrum esculentum) is a heteromorphic self-incompatible (SI) species with two types of floral architecture: thrum (short style) and pin (long style). The floral morphology and intra-morph incompatibility are controlled by a single genetic locus, S. However, the molecular mechanisms underlying the heteromorphic self-incompatibility of common buckwheat remain unclear. To identify these mechanisms, we performed proteomic, quantitative reverse-transcription PCR, and linkage analyses. Comparison of protein profiles between the long and short styles revealed a protein unique to the short style. Amino-acid sequencing revealed that it was a truncated form of polygalacturonase (PG); we designated the gene encoding this protein FePG1. Phylogenetic analysis classified FePG1 into the same clade as PGs that function in pollen development and floral morphology. FePG1 expression was significantly higher in short styles than in long styles. It was expressed in flowers of a short-homostyle line but not in flowers of a long-homostyle line. Linkage analysis indicated that FePG1 was not linked to the S locus; it could be a factor downstream of this locus. Our finding of a gene putatively working under the regulation of the S locus provides useful information for elucidation of the mechanism of heteromorphic self-incompatibility.</description><subject>Amino acids</subject><subject>Buckwheat</subject><subject>Fagopyrum - genetics</subject><subject>Fagopyrum - growth &amp; development</subject><subject>Fagopyrum esculentum</subject><subject>Flowers</subject><subject>Flowers - genetics</subject><subject>Flowers - growth &amp; development</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Genetic Linkage - genetics</subject><subject>Genetic Loci - genetics</subject><subject>Incompatibility</subject><subject>Linkage analysis</subject><subject>Loci</subject><subject>Molecular modelling</subject><subject>Morphology</subject><subject>Phylogeny</subject><subject>Plant Proteins - genetics</subject><subject>Pollen</subject><subject>Pollen - genetics</subject><subject>Pollen - growth &amp; development</subject><subject>Polygalacturonase</subject><subject>Polygalacturonase - genetics</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Self-incompatibility</subject><subject>Styles</subject><issn>0018-067X</issn><issn>1365-2540</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkc1u1DAUhSMEotPCA7BBlti0i8D1T2J7g1RVFCpVYgMSO8txnBkXxw52ApOn4JXxMKUCVrZ1zzm-R19VvcDwGgMVbzLDjPIasKyBEF7vH1UbTNumJg2Dx9UGAIsaWv7lpDrN-Q4AKCfyaXVCMfC2ZXJT_bzpbZjd4IyeXQwoDkijrQ0W2WBi78IWTdGvW-21mZcUg85ltJ-Szdn2KE_W_DZ7vyIXUN7FNKM8r97mw7t3h3tcMjJxHEt-t5ivP3ZWz-j8Wm_jtKZlRDabxZc1lvHiWfVk0D7b5_fnWfX5-t2nqw_17cf3N1eXt7VpKJ9raoA3PWuYltJ0pmEEbCt5a2AgA2G9EJpSjRuGB6BWMikaC7YjspN9NwhJz6q3x9xp6Ubbm_J70l5NyY06rSpqp_6dBLdT2_hdtVxg3JIScH4fkOK3xeZZjS4b670OtvRVhFAsgRc-RfrqP-ldXFIo9YpKiJY3AKKo8FFlUsw52eFhGQzqgFsdcauCWx1wq33xvPy7xYPjD1_6C0pAqqQ</recordid><startdate>20191001</startdate><enddate>20191001</enddate><creator>Takeshima, Ryoma</creator><creator>Nishio, Takeshi</creator><creator>Komatsu, Setsuko</creator><creator>Kurauchi, Nobuyuki</creator><creator>Matsui, Katsuhiro</creator><general>Springer Nature B.V</general><general>Springer International Publishing</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2525-7334</orcidid><orcidid>https://orcid.org/0000-0003-0965-2892</orcidid></search><sort><creationdate>20191001</creationdate><title>Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)</title><author>Takeshima, Ryoma ; Nishio, Takeshi ; Komatsu, Setsuko ; Kurauchi, Nobuyuki ; Matsui, Katsuhiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c537t-3c075d454a99cbc5420e6976c0f2f24d88a33a1541f03e94985e0eb29b9dbf893</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Amino acids</topic><topic>Buckwheat</topic><topic>Fagopyrum - genetics</topic><topic>Fagopyrum - growth &amp; development</topic><topic>Fagopyrum esculentum</topic><topic>Flowers</topic><topic>Flowers - genetics</topic><topic>Flowers - growth &amp; development</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Genetic Linkage - genetics</topic><topic>Genetic Loci - genetics</topic><topic>Incompatibility</topic><topic>Linkage analysis</topic><topic>Loci</topic><topic>Molecular modelling</topic><topic>Morphology</topic><topic>Phylogeny</topic><topic>Plant Proteins - genetics</topic><topic>Pollen</topic><topic>Pollen - genetics</topic><topic>Pollen - growth &amp; development</topic><topic>Polygalacturonase</topic><topic>Polygalacturonase - genetics</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Self-incompatibility</topic><topic>Styles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Takeshima, Ryoma</creatorcontrib><creatorcontrib>Nishio, Takeshi</creatorcontrib><creatorcontrib>Komatsu, Setsuko</creatorcontrib><creatorcontrib>Kurauchi, Nobuyuki</creatorcontrib><creatorcontrib>Matsui, Katsuhiro</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Heredity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Takeshima, Ryoma</au><au>Nishio, Takeshi</au><au>Komatsu, Setsuko</au><au>Kurauchi, Nobuyuki</au><au>Matsui, Katsuhiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)</atitle><jtitle>Heredity</jtitle><addtitle>Heredity (Edinb)</addtitle><date>2019-10-01</date><risdate>2019</risdate><volume>123</volume><issue>4</issue><spage>492</spage><epage>502</epage><pages>492-502</pages><issn>0018-067X</issn><eissn>1365-2540</eissn><abstract>Common buckwheat (Fagopyrum esculentum) is a heteromorphic self-incompatible (SI) species with two types of floral architecture: thrum (short style) and pin (long style). The floral morphology and intra-morph incompatibility are controlled by a single genetic locus, S. However, the molecular mechanisms underlying the heteromorphic self-incompatibility of common buckwheat remain unclear. To identify these mechanisms, we performed proteomic, quantitative reverse-transcription PCR, and linkage analyses. Comparison of protein profiles between the long and short styles revealed a protein unique to the short style. Amino-acid sequencing revealed that it was a truncated form of polygalacturonase (PG); we designated the gene encoding this protein FePG1. Phylogenetic analysis classified FePG1 into the same clade as PGs that function in pollen development and floral morphology. FePG1 expression was significantly higher in short styles than in long styles. It was expressed in flowers of a short-homostyle line but not in flowers of a long-homostyle line. Linkage analysis indicated that FePG1 was not linked to the S locus; it could be a factor downstream of this locus. Our finding of a gene putatively working under the regulation of the S locus provides useful information for elucidation of the mechanism of heteromorphic self-incompatibility.</abstract><cop>England</cop><pub>Springer Nature B.V</pub><pmid>31076649</pmid><doi>10.1038/s41437-019-0227-x</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-2525-7334</orcidid><orcidid>https://orcid.org/0000-0003-0965-2892</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0018-067X
ispartof Heredity, 2019-10, Vol.123 (4), p.492-502
issn 0018-067X
1365-2540
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6781162
source MEDLINE; Nature; EZB-FREE-00999 freely available EZB journals; PubMed Central; SpringerLink Journals - AutoHoldings
subjects Amino acids
Buckwheat
Fagopyrum - genetics
Fagopyrum - growth & development
Fagopyrum esculentum
Flowers
Flowers - genetics
Flowers - growth & development
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Plant - genetics
Genetic Linkage - genetics
Genetic Loci - genetics
Incompatibility
Linkage analysis
Loci
Molecular modelling
Morphology
Phylogeny
Plant Proteins - genetics
Pollen
Pollen - genetics
Pollen - growth & development
Polygalacturonase
Polygalacturonase - genetics
Proteins
Proteomics
Self-incompatibility
Styles
title Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum)
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T13%3A18%3A46IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Identification%20of%20a%20gene%20encoding%20polygalacturonase%20expressed%20specifically%20in%20short%20styles%20in%20distylous%20common%20buckwheat%20(Fagopyrum%20esculentum)&rft.jtitle=Heredity&rft.au=Takeshima,%20Ryoma&rft.date=2019-10-01&rft.volume=123&rft.issue=4&rft.spage=492&rft.epage=502&rft.pages=492-502&rft.issn=0018-067X&rft.eissn=1365-2540&rft_id=info:doi/10.1038/s41437-019-0227-x&rft_dat=%3Cproquest_pubme%3E2288675008%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2288675008&rft_id=info:pmid/31076649&rfr_iscdi=true